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Polygenic sex determination (PSD) may show variations in terms of genetic and environmental components between populations of fish species exposed/adapted to different environments. The European sea bass (Dicentrarchus labrax) is an interesting model, combining both a PSD system and a genetic subdivision into an Atlantic and a Mediterranean lineage, with genetic substructures within the Mediterranean Sea. Here, we produced experimental progeny crosses (N = 927) from broodstock sampled in four wild populations (North Atlantic, NAT; Western Mediterranean, WEM; North-Eastern Mediterranean, NEM; South-Eastern Mediterranean, SEM). We found less females than males in the progeny, both in the global dataset (32.5%) and within each paternal group (from 25.1% for NEM to 39.0% for WEM), with significant variation among populations, dams, and sires. Sex, body weight (BW), and body length (BL) showed moderate heritability (0.52 ± 0.17, 0.46 ± 0.17, 0.34 ± 0.15, respectively) and sex was genetically correlated with BW and BL, with r Asex/BW  = 0.69 ± 0.12 and r A sex/BL  = 0.66 ± 0.13. A weighted GWAS performed both on the global dataset and within each paternal group revealed a different genetic architecture of sex determination between Atlantic and Mediterranean populations (9 QTLs found in NAT, 7 in WEM, 5 in NEM, and 4 in SEM, with a cumulated variance explained of 27.04%, 21.87%, 15.89%, and 12.10%, respectively) and a more similar genetic architecture among geographically close populations compared to geographically distant populations, consistent with the hypothesis of a population-specific evolution of polygenic sex determination systems in different environments.

Population-specific variations of the genetic architecture of sex determination in wild European sea bass Dicentrarchus labrax L.